Ascorbate peroxidase postcold regulation of chloroplast NADPH dehydrogenase activity controls cold memory

Abstract

Exposure of Arabidopsis (Arabidopsis thaliana) to 4 °C imprints a cold memory that modulates gene expression in response to a second (triggering) stress stimulus applied several days later. Comparison of plastid transcriptomes of cold-primed and control plants directly before they were exposed to the triggering stimulus showed downregulation of several subunits of chloroplast NADPH dehydrogenase (NDH) and regulatory subunits of ATP synthase. NDH is, like PGR5-PGRL1 (Proton gradient 5–PGR5-like1), a thylakoid-embedded, ferredoxin-dependent plastoquinone reductase that protects photosystem I and stabilizes ATP synthesis by cyclic electron transport. Like PGRL1A and PGRL1B transcript levels, ndhA and ndhD transcript levels decreased during the 24 h long priming cold treatment. PGRL1 transcript levels were quickly reset in the post-cold phase, but expression of ndhA remained low. The transcript abundances of other ndh genes decreased within the next days. Comparison of tAPX-free and transiently tAPX-overexpressing or tAPX-downregulating Arabidopsis lines demonstrated that ndh expression is suppressed by post-cold induction of thylakoid-bound ascorbate peroxidase (tAPX). Four days after cold-priming, when tAPX protein accumulation was maximal, NDH activity was almost fully lost. Lack of the NdhH-folding chaperonin Crr27 (Cpn60β4), but not lack of the NDH activity modulating subunits NdhM, NdhO, or PnsB2 (Photosynthetic NDH subcomplex B2), strengthened priming regulation of ZAT10 (Zinc finger of Arabidopsis thaliana 10), which is a nuclear-localized target gene of the tAPX-dependent cold-priming pathway. We conclude that cold-priming modifies chloroplast-to-nucleus stress signalling by tAPX-mediated suppression of NDH-dependent cyclic electron transport and that plastid encoded NdhH, which controls subcomplex A assembly, is of special importance for memory stabilization.

Cold exposure transiently increases resistance ofArabidopsis thalianaagainst the fungal pathogenBotrytis cinerea

“…We suggest, that the stromal ROS protection with contribution from sAPX but without tAPX is sufficient to result in a wildtype-like plastid ROS homeostasis. In contrast, tAPX, but not sAPX, was identified as a specific mediator of cold priming-dependent altered activation of stress-related transcripts during a second cold exposure and affects cold priming-dependent regulation of chloroplast NADPH dehydrogenase activity (van Buer et al, 2016; van Buer et al, 2019; Seiml-Buchinger et al, 2022). Our ROS measurements (Fig.4) support the concept of distinct functions for sAPX and tAPX on plastid ROS control and redox signalling in response to cold pretreatments.…”

“…Stromal APX (sAPX) provides downstream antioxidant protection in the plastid stroma (Asada, 1999; Jardim-Messeder et al, 2022). Increasing evidence suggests that both plastid APX have additional functions in chloroplast energy metabolism and signalling (Kangasjarvi et al, 2008; Maruta et al, 2010; van Buer et al, 2016; Maruta et al, 2016; van Buer et al, 2019; Seiml-Buchinger et al, 2022). tAPX specifically regulates cold priming-mediated repression of core stress-responsive genes during a subsequent cold exposure (van Buer et al, 2019).…”

“…tAPX specifically regulates cold priming-mediated repression of core stress-responsive genes during a subsequent cold exposure (van Buer et al, 2019). In response to the initial cold, tAPX promotes the suppression of the chloroplast NADPH dehydrogenase subunits and alters chloroplast-to-nucleus stress signalling (Seiml-Buchinger et al, 2022). While tAPX transcripts decrease in the cold and slowly rise again during the post-cold phase, sAPX transcripts are upregulated in the cold and are quickly reset at normal growth temperatures (van Buer et al, 2016; Griebel et al, 2022).…”

Cold priming on pathogen susceptibility in the Arabidopsis eds1 mutant background requires a functional stromal Ascorbate Peroxidase

“… 35–38 In the priming control, tAPX-mediated suppression of chloroplast NADPH dehydrogenase subunits resulting in less cyclic electron transport provides a source for altered chloroplast-to-nucleus stress signaling. 39 While cold priming-reduced Pst susceptibility is significantly weakened in tapx-knockout (KO) lines compared to Col-0, Pst titers are similar in cold-pretreated and control sapx -KO (hereafter: sapx ) plants indicating a stronger contribution of sAPX. 9 …”